THE ANATOMICAL RECORD 290:507–513 (2007)

Anatomical Adaptations of Aquatic Mammals

JOY S. REIDENBERG* Center for Anatomy and Functional Morphology, Department of Medical Education, Mount Sinai School of Medicine, New York, New York

ABSTRACT This special issue of the Anatomical Record explores many of the an- atomical adaptations exhibited by aquatic mammals that enable life in the water. Anatomical observations on a range of fossil and living marine and freshwater mammals are presented, including sirenians (manatees and dugongs), cetaceans (both baleen whales and toothed whales, includ- ing dolphins and porpoises), pinnipeds (seals, sea lions, and walruses), the sea otter, and the pygmy hippopotamus. A range of anatomical sys- tems are covered in this issue, including the external form (integument, tail shape), nervous system (eye, ear, brain), musculoskeletal systems (cranium, mandible, hyoid, vertebral column, flipper/forelimb), digestive tract (teeth/tusks/baleen, tongue, stomach), and respiratory tract (larynx). Emphasis is placed on exploring anatomical function in the context of aquatic life. The following topics are addressed: evolution, sound produc- tion, sound reception, feeding, locomotion, buoyancy control, thermoregu- lation, cognition, and behavior. A variety of approaches and techniques are used to examine and characterize these adaptations, ranging from dissection, to histology, to electron microscopy, to two-dimensional (2D) and 3D computerized tomography, to experimental field tests of function. The articles in this issue are a blend of literature review and new, hy- pothesis-driven anatomical research, which highlight the special nature of anatomical form and function in aquatic mammals that enables their exquisite adaptation for life in such a challenging environment. Ó 2007 Wiley-Liss, Inc. Anat Rec, 290:507–513, 2007. Ó 2007 Wiley-Liss, Inc.

Key words: aquatic; adaptation; anatomy; marine mammal; sirenian; cetacean; pinniped; evolution

Aquatic life poses many challenges for mammals that 1975; Ridgway and Howard, 1979). A jointed, collapsible were originally adapted for life on land. As the evolution- rib cage allows compression of the thorax to accommo- ary process of natural selection can only apply to modify- date the shrinking lungs. Skeletal muscles are adapted ing present structures, aquatic mammals bring a lot of to maintain low levels of aerobic metabolism under the terrestrial baggage to their aquatic existence. For one hypoxic conditions associated with diving (Kanatous thing, they do not breathe water as fish do. Therefore, re- spiratory tract modifications are necessary to protect a system designed to function in air while excluding the *Correspondence to: Joy S. Reidenberg, Center for Anatomy ever-present surrounding water. Many of these adapta- and Functional Morphology, Department of Medical Education, tions have been previously described, for example, valvu- Mail Box 1007, Mount Sinai School of Medicine, 1 Gustave L. lar nostrils that exclude water, and an intranarial larynx Levy Place, New York, NY 10029-6574. (Reidenberg and Laitman, 1987) that further protects E-mail: [email protected] the respiratory tract from water inundation during swal- Received 13 March 2007; Accepted 13 March 2007 lowing. Diving presents additional challenges, as ambi- DOI 10.1002/ar.20541 ent pressure rises with increased depth. Lung volumes Published online in Wiley InterScience (www.interscience.wiley. collapse under the high pressures of a deep dive (Boyd, com).

Ó 2007 WILEY-LISS, INC. 508 REIDENBERG et al., 2002). Elevated levels of myoglobin in skeletal baleen, tongue, pharyngeal spaces, stomach), the exter- muscles also increase oxygen retention, thus enabling nal form (integument and body shape, including flukes longer dive times between breaths (Noren et al., 2001; and flippers), musculoskeletal systems (cranial, mandib- Wright and Davis, 2006). The mass of blood vessels ular, and cervical regions; postcranial axial and appen- located in the dorsum of the thorax (retia thoracica) have dicular skeleton), nervous system (eye, ear, brain), and been proposed to function during diving to accommodate respiratory tract (larynx). Emphasis is placed on explor- for the collapsed lung volume, thereby preventing gross ing anatomical function in the context of aquatic life. A displacement of abdominal organs (Hui, 1975). Salinity range of techniques are used, including dissection, histol- presents another challenge, as marine mammals must ogy, electron microscopy, computerized tomography and main water and salt balance, despite the frequent influx 3D reconstructions, and experimental field work. The of salt water they consume while swallowing prey. The papers that follow in this issue are a blend of both review kidney structure of cetaceans (whales, including dolphins articles and new, hypothesis-driven anatomical research. and porpoises) and pinnipeds (seals, sea lions, walruses) These studies highlight the dramatic anatomical changes is unusual, having a reniculate structure (Abdelbaki seen in the evolution from fossil ancestors to extant et al., 1984; Henk et al., 1986) not found in any other ter- aquatic mammals. This special issue is a tribute to the restrial mammals except bears, but does not appear to unique anatomical forms and functions of aquatic mam- have a greater ability to concentrate urine (Ortiz, 2001). mals that enables their adaptation to life underwater. Rather, the apparent advantage of numerous independ- ent renicules in marine mammals is limited tubule lengths in the necessarily large kidneys of gigantic mam- UNDERWATER FORAGING mals (Maluf and Gassman, 1998). The first question that naturally comes to mind is Navigation and prey detection systems are also modi- ‘‘Why did some mammals become aquatic in the first fied. As many aquatic mammals need to hunt at night place?’’ Uhen (2007, this issue) discusses the evolution of or in turbid or deep water, their sensory systems have aquatic mammals, using both molecular and morphologi- accordingly evolved. Pinnipeds developed longer and cal data for Cetacea, Sirenia, Desmostylia, and Pinnipe- more sensitive vibrissae that can pick up hydrodynamic dia. He notes that re-entering the water occurred on at trails (vibrations in water) of fish swimming, or relay in- least seven different occasions. Specific changes occurred formation about water current flow and variations in in the axial and appendicular skeleton that improved substrate surfaces (Dehnhardt et al., 2001). Odontocetes locomotion for aquatic foraging. Nostril, eye placement, (toothed whales) developed nasal structures that gener- rostrum, and dental morphology also changed, depend- ate echolocation, enabling them to use sound to locate ing upon the need to forage while wading versus sub- prey or navigate past obstacles (Cranford et al., 1996; mersion. Although the end product of each of these evo- Au et al., 2006). lutionary trajectories is vastly different, they all appear Many marine mammals have modified their external to be the result of natural selection for improved aquatic shape, developing new propulsion mechanisms for loco- foraging. Terrestrial mammals from seven separate line- motion in water. Seals use alternating horizontal sweeps ages thus re-invaded the water to fill a vacant niche: of their hind flippers (Fish et al., 1988). Fur seals and feeding in water. sea lions ‘‘fly’’ underwater by beating their fore flippers The foraging mechanisms of fossil ancestors, however, (English, 1977; Feldkamp, 1987). Walruses sometimes do not always match present day species. Domning and use their tusks to grip the sea floor or ice and push their Beatty (2007, this issue) compare fossil and modern body forward with a downward nod of the head. Sire- dugongs in their tusk shape and cranial anatomy, and nians (manatees and dugongs) have lost their hind explore whether these specializations indicate tusk use limbs, but can either propel themselves with their tail in feeding. Fossil dugongines exhibit cranial modifica- fluke(s) or walk along the sea or river floor with their tions that may have assisted downward and backward forelimbs. Cetaceans have excelled in the attainment of tusk cutting motions. The larger, more blade-like tusks streamlined form, and are thus the fastest swimmers. of fossil dugongines are more effective at harvesting rhi- As with sirenians, cetaceans have lost appendages that zomes. However, examination of microwear patterns in detract from axial locomotion (hind limbs). Similarly to modern dugong tusks do not support that their use is pinnipeds, they have modified extremities that assist necessary in feeding, although it does occasionally occur with lift and braking (flippers). Cetaceans have also in large adult males. Tusk use in modern dugongs has added new extensions that aid propulsion (flukes) or pre- thus changed radically from the ancestral pattern. As vent roll or yaw (dorsal fin) while swimming with exag- tusks are not essential for feeding in extant dugongs, the gerated pitch (dorsoventral bending). persistence of erupted tusks in males indicates a possible Although most of the above-mentioned adaptations role in sexual selection or other social interactions. have been discussed at length in previous publications, Feeding mechanisms are also examined in cetaceans in the articles in this special issue present some new find- this issue. MacLeod et al. (2007, this issue) describe the ings regarding aquatic adaptations. This special issue relationship between prey size and skull asymmetry. focuses on a common hypothesis: the described anatomi- While most mammals are bilaterally symmetrical, most cal specialization confers a selective advantage to an odontocetes are characterized by directional asymmetry aquatic existence. Demonstrating this relationship neces- of the skull (i.e., the direction of deviation is consistent). sarily involves exploring how the adaptation functions in The narial apertures are asymmetrically positioned on an aquatic environment. The studies presented examine the left side of the head (Yurick and Gaskin, 1988). Above a large array of extant and fossil, marine and fresh the skull, this asymmetry is also evident in soft tissue water, aquatic mammals. A variety of anatomical sys- structures that are used in generating echolocation sig- tems are explored, including digestive tract (teeth, tusks, nals (Cranford et al., 1996). The different sized nasal ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS 509 diverticulae, fat bodies, and valvular flaps may enable pleats), expand the floor of the oral cavity to engulf generation of two different sounds simultaneously. While water containing schools of small fish or krill, and then this asymmetry may be useful for echolocation signal gen- expel water through their baleen plates. The baleen eration, it is suggested that echolocation is an overlay on serves as a filter, allowing water to pass through while asymmetry developed initially in conjunction with feeding trapping the small prey. These whales need a highly mo- needs. Below the skull, the left-shifted nares correspond bile tongue that can flatten and expand to accommodate to a left-shifted larynx. A larynx positioned asymmetri- the distention of the oral cavity. The tongue may also cally on the left side collapses the left piriform sinus (lat- aid in wiping prey off of the baleen plates. eral food channel, but simultaneously provides a larger Although baleen is an aquatic adaptation that enables piriform sinus on the right side; Reidenberg and Laitman, filter feeding, it has an additional use in humpback 1994). This should enable asymmetric odontocetes to whales. Air (technically, gas) from the respiratory tract swallow larger prey than their symmetric counterparts. may be released into the oral cavity and then pushed out MacLeod et al. (2007, this issue) test this hypothesis by through the sieve of the baleen plates, resulting in an examining the relationship between skull asymmetry rel- underwater visual display called a bubble cloud (Reiden- ative to skull size and maximum relative prey size con- berg and Laitman, 2007a, this issue). Gas is released sumed. The strong positive correlation indicates that as from the respiratory tract by removing the epiglottis of odontocete nasal asymmetry increases, so does the size of the larynx from its normal position behind the soft pal- the prey they can consume. This is an obvious adaptation ate, and instead inserting it into the oral cavity. Gas can to feeding in general, and to aquatic existence in particu- then flow from the lungs, trachea, or laryngeal sac into lar, as odontocetes swallow their prey whole without proc- the oral cavity. As the floor of the mouth is contracted, essing. Therefore, more energy is gained by consuming and the gape of the mouth is held nearly closed, gas is one large prey item for the same amount of effort as is forced superiorly and laterally against the racks of ba- expended to catch one small prey item. leen. The criss-crossing fibers on the lingual surface of Underwater feeding poses an additional challenge: the stacked baleen plates serve to break up the gas pass- predators need to engulf prey while sorting it from the ing through it into many small bubbles, which give the surrounding aquatic milieu. In cetaceans, movements of appearance of a fine, white mist underwater. This behav- the hyoid apparatus play an important role in both ior is surprising, as it risks the protective arrangement of drawing prey into the oral cavity and enlarging the piri- the intranarial larynx designed to keep water out of the form sinus (particularly on the right side) for swallowing respiratory tract. It is thus perhaps a unique example of prey whole (Reidenberg and Laitman, 1994). In addition, an aquatic adaptation that compromises another aquatic the tongue plays an important role in squeezing water adaptation. Despite this risk, there are many potential out of the mouth. Werth’s (2007, this issue) study of the advantages to generating such a display. Bubble clouds hyolingual apparatus, particularly the tongue, in ceta- may be a signal to conspecifics swimming close by—par- ceans shows aquatic specializations that relate to ther- ticularly in water with good visibility such as is found in moregulation. There are counter current vessels in the the tropical areas where mating usually occurs. The bub- tongue that control heat loss to the water in the oral bles may also help herd prey into a tighter schooling for- cavity. Species-specific differences in musculoskeletal mation, making it easier to engulf larger numbers of features of the hyolingual apparatus are related to the prey during feeding. In addition, bubble clouds may be mode of feeding used: suction, raptorial prehension, con- used as camouflage. In open water, there are no obstacles tinuous filtering, and engulfing with straining. Odonto- to hide behind. A bubble cloud may thus provide a visual cetes have a small, rigid mouth, enlarged hyoid appara- barrier (similar to a bush or a smoke screen), that can tus, and hypertrophied tongue muscles. Grasping prey is block a predator’s view of the whale while it takes eva- much like the game ‘‘bobbing for apples’’—and old-fash- sive action. In addition, the bubbles may serve as an ioned New England tradition in which a person dunks echoic barrier to predatory orcas, causing disruption or their face into a bucket of water with floating apples distortion of their echolocation signal (similar to a white and tries to grasp one with their teeth. In most cases, noise generator or a sonar jamming device). the smooth-sided apple eludes capture because it simply The exploration of digestive tract anatomy continues slides out of the grasp of the teeth and forward of the in this special issue with an examination of the stomach water pressure generated by the closing mouth. Odonto- in the Ziphiidae, the family of rare beaked whales. Mead cetes, faced with a similar problem while feeding under- (2007, this issue) describes three morphological appear- water, developed a unique mechanism to trap slippery ances of the stomach: generalized ziphiid stomach (1 prey (e.g., fish, squid) in their mouth. They use their main stomach, 1 pyloric stomach), derived stomach type hyoid and tongue as a piston: a sudden retraction gener- I (2 main stomachs, 1 pyloric stomach), and derived ates negative pressure in the mouth which, in turn, stomach type II (2 main stomachs, 2 pyloric stomachs). draws prey into the oral cavity. In some cetaceans, the A multiple chambered stomach is unusual in carnivores. large tongue is also used for grasping and manipulating However, although all cetaceans are carnivores, the prey. Mysticetes (baleen whales) use two different modes presence of a multichambered stomach should not sur- of filter feeding. Balaenid mysticetes (right and bowhead prise us. Whales are, afterall, closely related to artiodac- whales) are continuous strainers. They swim forward tyls, which also have multichambered stomachs. While with their mouth open, constantly taking in water with their multiple chambers may relate to the mechanical small prey at the front of the mouth while streaming and enzymatic breakdown of an herbivorous diet (e.g., excess water out of the lateral–caudal edge of the gape. separation of food to be regurgitated and re-chewed as Their tongue is larger and stiff, and may function to cud), it is unclear what functions multiple chambers direct water flow through the mouth. Balaenopterid play in the carnivorous ziphiids. Nevertheless, differen- mysticetes (rorqual whales, which possess ventral throat ces in the appearance of the three stomach morphologies 510 REIDENBERG appear to be useful for elucidating systematic relation- tion between the epidermis and the dermis, a fat-free ships among the ziphiids. zone of collagen fibers in the reticular dermal layer, and elastic fiber networks within the dermal and hypodermal EXTERNAL ANATOMY: INTEGUMENT AND layers. These features may reduce hydrodynamic fric- tion, enabling the skin to deform under pressure to BODY SHAPE increase hydrodynamic flow of water over the body dur- One obvious place to discover adaptations to an ing high speed swimming. aquatic existence is to look at the point of contact between the aquatic environment and the aquatic mam- mal. Therefore, the integument and overall body shape LOCOMOTION is examined in this special issue. Fur originally func- The thicker substrate of water creates resistance to tioned as a terrestrial modification to trap an insulating locomotion compared with air, thus necessitating the layer of air, providing camouflage, protection from abra- need for a fusiform body shape that decreases drag in sion or predatory injury, or shielding from the untravio- pelagic marine mammals. Aquatic adaptations can also let rays of the sun. Fur in water, while providing all of be seen in the hydrodynamic shapes of the structures the latter features, loses it ability to insulate and also used to generate thrust in cetaceans: tail flukes. Fish generates increased drag while swimming. Aquatic et al. (2007, this issue) uses CT scans to describe the mammals thus have developed oily furs that are rela- thickness ratios of cetacean flukes. He found that their tively waterproof (e.g., polar bears, otters, seals, sea shape was effective at reducing drag while moving at lions, beavers). Their fur may trap air, thus continuing high speeds. Fluke shapes were also found to be ideal to provide insulation even when wet. In some aquatic for reducing the tendency for flow to separate from the mammals, fur was lost in favor of a thicker, waterproof fluke surface. This feature, combined with the relatively epidermis (e.g., whales, dolphins, porpoises, manatees, large leading edge radius, results in a shape that gener- dugongs, walruses, hippopotomi). This change may be a ates greater lift and helps to delay stall. Interestingly, response to hydrodynamic needs, such as drag reduction. cetacean flukes were better at generating lift than engi- The loss of air trapping for insulation necessitated the neered foils, thus showing that we still have a lot to development of thickened fat layer called blubber. learn from nature. Vascular plexuses also developed to enable counter Sirenians also use a tail for propulsion which, simi- current exchange, which conserves body heat centrally larly to cetaceans, consists of a fluke (or flukes) that are while allowing the periphery to remain cold. Cold is not supported only by a midline skeleton of caudal verte- the only thermal disadvantage to living in the water, brae. Dugongs have two mirror-image flukes, similar in however. Heat can also build up in overly insulated shape to the double flukes of cetaceans. Manatees have mammals when the ambient temperature rises at the a single, paddle-shaped fluke. Of interest, the evolution water’s surface or, in the case of semiaquatic mammals of tail flukes in sirenians is convergent with the evolu- (e.g., pinnipeds), while on land. Heat dissipation is also tion of tail flukes in cetaceans. Buchholtz et al. (2007, necessary during exertion or during pregnancy. Vascular this issue) indicates that fluke evolution developed adaptations channel excess heat from locomotor muscles before the separation of manatees and dugongs. or the reproductive organs to large flat surfaces (flukes, Caudal propulsion in manatees is facilitated by flippers, fin) which act as radiators (Rommel et al., 1992, changes in both the shape and number of bones in the 1993, 1995, 2001). Oral rete allow cetaceans to regulate axial skeleton. Buchholtz et al. (2007, this issue) heat loss from the oral cavity (Werth, 2007, this issue). describe the anatomy of the Florida manatee vertebral Changes in body shape also contribute to heat conser- column in comparison to those of African manatees and vation/radiation. Terrestrial mammals living in cold envi- dugongs. Manatee vertebral counts and morphology are ronments tend to have shortened extremities (e.g., limbs, unusual compared with both terrestrial mammals and ears, muzzles) to restrict heat radiation, while the oppo- other sirenians. Aquatic adaptations can be seen in the site is true in hot environments. There are several exam- compressed cervical and elongate thoracic vertebrae, ples of cold water adapted marine mammals that also dis- short neural spine length, variation and reduction of the play shortened extremities and rotund body shapes (e.g., lumbus, low precaudal count, lack of a sacral series, and walrus, bowhead whale, right whale, beluga whale). discontinuity within the caudal series. These traits all Reeb et al. (2007, this issue) examine the integument contribute to aquatic locomotion. The shortened neck of the southern right whale, one of the cold water limits head mobility, decreases drag, and effectively adapted marine mammals. Southern right whales have repositions the flippers more anteriorly. Reduction in hairs, but they no longer function to trap air. Rather, precaudal vertebrae count and elongation of dorsal ver- they may have a tactile function and are probably used tebrae lowers the number of intervertebral flexion as vibrissae to detect changes in prey density. Epidermal points, thus stabilizing the column while elongating the specializations (e.g., callosities) provide barriers against body. Short neural spines and flat centrum faces also mechanical injury. There were lipid droplets associated decrease vertebral flexion and increase stability. Caudal with the nucleus, which may facilitate the energetics of vertebrae have smaller centra and neural spines, which nuclear metabolism. This may be an adaptation to sup- increase flexibility, and small posteriorly inclined trans- port cellular metabolism during extreme cold exposure verse processes, which serve as an anchor for muscles of (e.g., deep diving, polar waters) when the arterial supply locomotion. Rounded centrum faces, absent zygapophy- of nutrients to the skin is reduced to conserve heat. Not ses, and reduction of both neural spines and transverse surprisingly, these whales also have a thick, insulatory processes facilitate flexibility in the fluke region, a trait integument, which acts as a thermoregulatory adapta- necessary for caudal propulsion. These traits enable tion to a cold environment. There is a highly folded junc- axial locomotion, specifically dorsoventral bending. ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS 511 Changes in buoyancy are a challenge for aquatic loco- their fore and hind flippers to walk and even run on motion: a shallow-water wading or bottom-feeding ani- land. Seals, however, do not usually use their extremities mal needs to be heavier than water to retain traction on on land. Rather, they use an unusual rolling motion, pro- the substrate (e.g., moose) or stay submerged to feed pelling their body forward through the progression of a (e.g., manatee), an animal living at the surface needs to dorsoventral body wave—similar to the alternating side- float (e.g., sea otter), and an open-water free-swimming ways movements of a snake, but turned 90 degrees into animal needs to be neutrally buoyant to rise and fall the vertical plane. Their movement is reminiscent of the within the water column (e.g., dolphin). Gray et al. up-and-down body wave many aquatic mammals use to (2007, this issue) discuss the evolution of buoyancy con- swim underwater (e.g., dolphins, manatees). Nonflip- trol mechanisms as evidenced by microstructural pered aquatic mammals that have retained four weight- changes in the skeletal system, from analysis of ribs in bearing limbs (e.g., polar bear, otter, beaver, muskrat) five fossil cetacean families. Paradoxically, this aquatic can walk on land with a quadrupedal gait similar to their specialization predates gross anatomical changes associ- fully terrestrial relatives (Tarasoff et al., 1972). Some ated with swimming in archaeocetes. There was a shift mammals limit their aquatic exposure only to wading in from the typical terrestrial form, to osteopetrosis and water (e.g., moose). This allows them to reduce the pachyosteosclerosis, and then to osteoporosis in the first effects of friction by keeping their trunk out of the water quarter of cetacean evolutionary history. High bone den- (enabled by having long limbs) and reducing the surface sity is a static buoyancy mechanism that provides bal- area of the limbs (i.e., skinny legs). Hippos, however, last and is found in bottom feeders such as sirenians. keep most of their body submerged while in water and Low bone density is associated with dynamic buoyancy have rather thick extremities. control mechanisms (e.g., amount of gas in the lungs), Fisher et al. (2007, this issue) discuss adaptations in and is found in mammals living in deep water. forelimb of the pygmy hippo that enable them to move Appendicular osteology is also highly modified in quickly in water despite their rotund habitus. Unlike aquatic mammals. Unlike caudal flukes, which only most other aquatic mammals, pygmy hippos do not have midline skeletal support, the external form of a swim, but rather walk on muddy substrates. Propelling flipper is dependent upon its underlying skeletal struc- the trunk through the high frictional resistance of water ture. Flipper shape reflects functional locomotor require- thus requires robust musculature, compared with that of ments to increase lift, reduce drag, execute turns, and quadrupedal land mammals such as the closely related enable braking. Narrow, elongate flippers facilitate fast artiodactyls. In addition, pygmy hippos bear weight on swimming while broad flippers aid in slow turns. Cooper all of their toes and can prevent the toes from splaying. et al. (2007, this issue) show that digit loss and digit These adaptations enable them to walk on the soft sur- positioning appear to underlie these disparate flipper faces of a muddy substrate, as is found on the bottoms shapes. The osteology of the cetacean flipper (consisting or edges of lakes or rivers. Hippos retain several primi- of the humerus, radius, ulna, carpals, metacarpals, and tive muscles, thus indicating their early evolutionary phalanges) also provides many clues regarding their evo- divergence from Artiodactyla. This divergence may also lution from a terrestrial ancestor with five digits. Cooper be closely allied to the divergence of Cetacea, thus et al. (2007, this issue) describe differences in the num- explaining the molecular data linking hippos and ceta- ber of digital rays in the two suborders of mysticetes ceans as closely related groups. and odontocetes. Digital ray I is reduced in most penta- dactylous cetaceans and is completely lost in tetradacty- BRAIN, EYE, AND COMMUNICATION lous mysticetes. Five digits help support a broad flipper (e.g., right whales), while four digits closely appressed SYSTEMS are seen in narrow, elongated flippers (e.g., humpback Cetaceans possess among the largest brains, both in whales). Most odontocetes also reduce the number of absolute mass and relative to body size. It has been sug- phalangeal elements in digit V, while mysticetes typi- gested that the large brains are an aquatic adaptation, cally retain the plesiomorphic condition of three pha- particularly in echolocating odontocetes. Marino (2007, langes. All cetaceans, however, exhibit an increased this issue) addresses this relationship in a study compar- number of phalanges (hyperphalangy). Hyperphalangy ing brain size (as measured by encephalization quotient, and associated multiple interphalangeal joints may which accounts for body size) in fossil and modern smooth the leading edge contour of the flipper, thereby aquatic mammals. She concludes that brain size is inde- helping to distribute leading edge forces. pendent of aquatic existence, as large brains developed in Flippers are also found in other marine mammals, cetaceans well after they became aquatic. Furthermore, including sirenians and pinnipeds. Sirenians may use other aquatic mammals (e.g., pinnipeds, sirenians) do not them to crawl along the river bed or the sea floor. Unlike possess markedly enlarged brains, complex gyrification cetaceans and sirenians, the pinnipeds are among the patterns, or high encephalization levels compared with group of amphibious mammals (i.e., mammals that regu- odontocete brains. Echolocation alone cannot account for larly leave the water for extended periods of time). As all of these changes, as terrestrial echolocators (e.g., bats) such, these aquatic mammals must adapt to the change are not highly encephalized. Rather, Marino postulates in substrate while entering or exiting water, and thus that the high encephalization level of odontocetes is more retain the ability to locomote both on land and in water. likely related to their complex social structure. Sea lions, walruses, and seals all possess both fore and While brain size may not reflect aquaticism, other hind flippers that contain many of the same, although nervous tissues do. The eye, which is technically an highly modified, musculoskeletal elements as terrestrial extension of the brain, exhibits several specializations in forelimbs (English, 1976). Sea lions, despite their highly aquatic mammals. Mass and Supin (2007, this issue) modified extremities, can still raise themselves on both review eye anatomy in four aquatic groups: cetaceans, 512 REIDENBERG pinnipeds, sirenians, and sea otters. They found anatom- sound source has remained undescribed for mysticetes. ical differences that correspond to species-specific While vocal fold homologs have been identified in odonto- aquatic adaptations and behaviors. Aquatic mammals cetes (Reidenberg and Laitman, 1988), vocal folds were use different mechanisms to achieve aerial versus sub- thought to be absent in baleen whales. Homology was merged emmetropia (refraction of light to focus on the determined by criteria that define vocal folds in terres- retina). These corrections occur due to species-specific trial mammals. The vocal fold homologue is described as differences at the cornea or the lens. Pupil shapes corre- a U-shaped fold that is (1) able to function as a valve to spond with variations in depth-dependent light expo- regulate gas flow, (2) supported by arytenoid cartilages, sure. Retina composition is similar to nocturnal terres- (3) controlled by muscles that either directly insert on it trial mammals, which is not surprising because aquatic or move the arytenoid cartilages, (4) is connected across mammals are exposed to low light conditions under- the midline by a ligament, (5) receives motor and sensory water. Cetaceans exhibit two areas of ganglion-cell con- innervation from the recurrent laryngeal nerve for the centration (the best-vision areas) located in the temporal controlling musculature and mucosa caudal to the fold, and nasal quadrants, while pinnipeds, sirenians, and and sensory innervation from the superior laryngeal sea otters have only one such area. nerve for the mucosa rostral and ventral to the fold, and Aquatic specializations are also apparent in the hear- (6) is located adjacent to a diverticulum called the laryn- ing apparatus of aquatic mammals. The terrestrial ear geal sac (likely derived from the laryngeal ventricles). depends upon sound waves in air being collected by the Unlike the vocal folds of terrestrial mammals, which are pinna, traveling though the auditory meatus, causing perpendicular to airflow, the mysticete U-fold is oriented vibrating of a tympanic membrane. These vibrations are parallel to airflow. In this position, it can regulate airflow then transmitted through an ossicular chain to the oval into/out of the laryngeal sac, and vibration of its edges window, where vibrations set the inner ear membranes may generate sounds. The size and complexity of the and fluid into motion, causing bending of hair cells, mysticete larynx indicates an organ with multiple func- which in turn, transmit an electrical signal that the tions in addition to sound generation, including protec- brain interprets as sound. Underwater hearing poses tion during breathing/swallowing, and airflow/gas pres- technical challenges, as sound waves are propagated in a sure control in the respiratory spaces. fluid medium. Submerged terrestrial mammals primarily hear through bone conduction. However, as terrestrial ears are not acoustically isolated from the skull, they CONCLUSIONS cannot distinguish directionality of sound under water. The articles in this special issue draw from several an- Nummela at al. (2007, this issue) describe the evolution atomical disciplines to present both the latest discoveries of underwater hearing in cetaceans, particularly the in aquatic mammal research as well as some thoughtful sound transmission mechanisms in six archaeocete fami- and thorough evolutionary and systems-based reviews. lies. They show that the pinna and external auditory me- It is hoped that, after reading this collection, one will atus were replaced by the mandible and its associated fat have a greater understanding of how much these ani- pad, which transmit sound pressures to the tympanic mals have changed through the effects of natural selec- plate (lateral wall of the bulla). Other changes include tion from their terrestrial ancestors, through the various medial thickening of the tympanic bulla, functional fossil intermediate forms to the diversity of extant replacement of the tympanic membrane by a bony plate, aquatic mammals we have today. Knowledge of their un- and changes in the orientation and shapes of the ossicles. usual specializations will hopefully inspire us to copy na- In addition, the tympanoperiotic complex becomes acous- ture in the development of new technologies. For exam- tically isolated from the skull by means of the develop- ple, continued investigations on flukes, flippers, axial ment of air sinuses. This acoustic isolation prevents bony movements, feeding mechanics, skin, and body shape conduction and, therefore, preserves stereo hearing by may lead to development of more efficient hydrodynamic means of mandibular transmission. designs for water- and aircraft. Further study of how Hearing sensitivity is examined in a particularly rare aquatic mammals regulate buoyancy, control bone den- cetacean, the North Atlantic right whale. As traditional sity, or manage dramatic changes in temperature and behavioral or physiological hearing tests are not feasible pressure as they rise and fall in the water column may with right whales, a functional model was developed lead to new treatments for osteoporosis or the invention based upon the ear anatomy. Parks et al. (2007, this of protective gear for exposure to the extreme environ- issue) examined right whale ears by means of histologic mental changes of high and low altitude, space, or ocean measurements of the basilar membrane and 2D and 3D depths. A more complete understanding of neural orga- computerized tomography reconstructions of the cochlea. nization, underwater vision, or sound generation and An estimated hearing range of 10 Hz–22 kHz based on sound reception mechanisms may lead to the creation of established marine mammal models was obtained. This better artificial sensory systems. There is so much we knowledge of the sound reception abilities of right still have to learn about aquatic mammals. This is an whales is an important beginning to understanding their exciting time to be a marine mammal scientist. acoustic communication system and possible impacts of A brief note about conservation. Many of the aquatic anthropogenic noise. mammals discussed in this issue are critically endan- The last article of the special issue addresses the other gered. Unfortunately, people only protect what they end of the communication spectrum: sound generation. know. Publications such as this, however, enable us to Reidenberg and Laitman (2007b, this issue) describe the fulfill our duty as scientists to help educate the public discovery of a mysticete homolog of the vocal folds (the with scientific facts about these splendid animals. After structures responsible for sound production in terrestrial reading about all the phenomenal adaptations of aquatic mammals). This is a particularly exciting finding, as the mammals presented here, I hope you will join me not ANATOMICAL ADAPTATIONS OF AQUATIC MAMMALS 513 only in a new appreciation for how special these animals muscles of Weddell seals: key to longer dive durations? J Exp Biol truly are, but also in a renewed commitment to help pro- 205:3601–3608. tect them from extinction. MacLeod CD, Reidenberg JS, Weller M, Santos MB, Herman J, Goold J, Pierce GJ. 2007. Breaking symmetry: the marine envi- ronment, prey size and the evolution of asymmetry in Cetacean ACKNOWLEDGMENTS skulls. Anat Rec (this issue). I thank the contributors to this issue for all their hard Maluf NS, Gassman JJ. 1998. Kidneys of the killerwhale and signif- work in producing outstanding pieces. I am in debt to icance of reniculism. Anat Rec 250:34–44. those reviewers who spent numerous hours reviewing Marino L. 2007. Cetacean brains: how aquatic are they? Anat Rec (this issue). and providing helpful critiques of the papers, thereby Mass AM, Supin AYa. 2007. Adaptive features of the aquatic mam- vastly improving the content of this special issue. A spe- mals’ eye. Anat Rec (this issue). cial thank you goes to the editor, Kurt Albertine, for Mead J. 2007. Stomach anatomy and use in defining systemic rela- encouraging and promoting publication of high quality, tionships of the cetacean family Ziphiidae (beaked whales). Anat hypothesis-driven anatomical research. My deepest grat- Rec (this issue). itude goes to Jeff Laitman, Associate Editor, for his Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL. 2001. invaluable guidance, helpful advice, immeasurable sup- The development of diving in marine endotherms: preparing the port, abounding encouragement, and enthusiastic faith skeletal muscles of dolphins, penguins, and seals for activity dur- in my ability to ‘‘pull off’’ this endeavor. He continues to ing submergence. 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